Available online at www.sciencedirect.com Geochimica et Cosmochimica Acta 74 (2010) 3232–3245 www.elsevier.com/locate/gca Formation of nano-crystalline todorokite from biogenic Mn oxides Xiong Han Feng a,1, Mengqiang Zhu a, Matthew Ginder-Vogel a,b, Chaoying Ni c, Sanjai J. Parikh a,2, Donald L. Sparks a,b,* a Environmental Soil Chemistry Research Group, Department of Plant and Soil Sciences and Center for Critical Zone Research, 152 Townsend Hall, University of Delaware, Newark, DE 19716, USA b Delaware Environmental Institute, University of Delaware, Newark, DE 19716, USA c Department of Materials Science and Engineering, 201 Dupont Hall, University of Delaware, Newark, DE 19716, USA Received 15 May 2009; accepted in revised form 3 March 2010; available online 12 March 2010 Abstract Todorokite, as one of three main Mn oxide phases present in oceanic Mn nodules and an active MnO6 octahedral molec- ular sieve (OMS), has garnered much interest; however, its formation pathway in natural systems is not fully understood. Todorokite is widely considered to form from layer structured Mn oxides with hexagonal symmetry, such as vernadite (d-MnO2), which are generally of biogenic origin. However, this geochemical process has not been documented in the environment or demonstrated in the laboratory, except for precursor phases with triclinic symmetry. Here we report on the formation of a nanoscale, todorokite-like phase from biogenic Mn oxides produced by the freshwater bacterium Pseudomonas putida strain GB-1. At long- and short-range structural scales biogenic Mn oxides were transformed to a todorokite-like phase at atmospheric pressure through refluxing. Topotactic transformation was observed during the trans- formation. Furthermore, the todorokite-like phases formed via refluxing had thin layers along the c* axis and a lack of c* periodicity, making the basal plane undetectable with X-ray diffraction reflection. The proposed pathway of the todorok- ite-like phase formation is proposed as: hexagonal biogenic Mn oxide ? 10-A˚ triclinic phyllomanganate ? todorokite. These observations provide evidence supporting the possible bio-related origin of natural todorokites and provide important clues for understanding the transformation of biogenic Mn oxides to other Mn oxides in the environment. Additionally this method may be a viable biosynthesis route for porous, nano-crystalline OMS materials for use in practical applications. Ó 2010 Elsevier Ltd. All rights reserved. 1. INTRODUCTION Mn oxides are environmentally ubiquitous and an important source of reactive mineral surfaces in the envi- * Corresponding author at: Environmental Soil Chemistry ronments. There are over 30 known Mn oxide/hydroxide Research Group, Department of Plant and Soil Sciences and minerals resulting from the numerous environmental Mn Center for Critical Zone Research, 152 Townsend Hall, University oxidation states [Mn(II), Mn(III) and Mn(IV)] and an array of Delaware, Newark, DE 19716, USA. Tel.: +1 302 831 6378; fax: of atomic arrangements (McKenzie, 1989; Dixon and Skin- +1 302 831 0605. ner, 1992; Post, 1999). These minerals participate in a vari- E-mail address: [email protected] (D.L. Sparks). 1 ety of chemical and biological reactions that affect the water Present address: College of Resources and Environment, quality of marine and soil systems (Villalobos et al., 2003; Huazhong Agricultural University, Wuhan 430070, PR China. Tebo et al., 2004; Webb et al., 2005a), and due to their reac- 2 Present address: Department of Land, Air and Water Resources, One Shields Avenue, The University of California, tivity have been called “scavengers of the sea” (Goldberg, Davis, CA 95616, USA. 1954). The basic building block of Mn oxides is the 0016-7037/$ - see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.gca.2010.03.005 Formation of todorokite from biogenic Mn oxides 3233 MnO6 octahedron. These octahedra can be assembled ally possessed a layered topology (Saratovsky et al., through corner and/or edge sharing into a variety of struc- 2006). In the presence of U(VI) the marine bacterium Bacil- tures that fall into two basic categories: (1) layer structures lus sp. strain SG-1 forms poorly ordered Mn oxide tunnel (phyllomanganates) and (2) chain, or tunnel structures (tec- structures, similar to todorokite (Webb et al., 2006); how- tomanganate) (McKenzie, 1989; Dixon and Skinner, 1992; ever, this phase has not been identified in environmental Post, 1999). According to the tunnel size, tectomanganates systems. Synthetic todorokites are generally obtained from can be denoted as T(m  n). Todorokite, a family of tunnel modifying a layer structured Mn oxide with triclinic sym- structure Mn oxides with a T(3  3) array of edge-shared metry via a hydrothermal chemical route at relatively high MnO6 octahedra, is commonly associated with ferromanga- temperature and pressure (Golden et al., 1986; Shen et al., nese oxides from marine (Burns and Burns, 1978a; Chukh- 1993; Feng et al., 1995, 1998; Vileno et al., 1998; Ching rov et al., 1979; Mellin and Lei, 1993; Takahashi et al., et al., 1999; Luo et al., 1999; Liu et al., 2005). The forma- 2007) and terrestrial (Turner and Buseck, 1981; McKeown tion of todorokite is greatly accelerated under mild reflux and Post, 2001; Manceau et al., 2007) settings. Mn oxide conditions at atmospheric pressure, enabling the simulation minerals are of potential economic interest because they of formation processes for naturally occurring todorokite are often enriched in Co, Ni, Cu and other strategic metals, (Feng et al., 2004; Cui et al., 2006, 2008, 2009a,b). Here including platinum group and rare earth elements (Post, we describe the transformation of biogenic Mn oxide into 1999; Glasby, 2006). In addition, todorokite has many po- a todorokite-like phase. The transformation products were tential industrial applications, including use as sorbents, characterized using X-ray absorption near edge structure heterogeneous catalysts, sensors, and rechargeable battery (XANES) and extended X-ray absorption fine structure cathodes (Shen et al., 1993; Vileno et al., 1998; Ching (EXAFS) spectroscopies, synchrotron-based X-ray diffrac- et al., 1999; Feng et al., 1999; Suib, 2008; Cui et al., 2009a). tion (SR-XRD), transmission electron microscopy (TEM), Many of these Mn oxides are formed by microbial oxi- field emission gun scanning electron microscopy (FEG-SEM) dation of soluble Mn(II). In fact Mn-oxidizing biota (i.e., and high-resolution transmission electron microscopy bacteria and fungi) are commonly distributed throughout (HR-TEM). We also propose a potential transformation freshwater, ocean, and soil environments and catalyze the pathway and mechanism for biogenic Mn oxides transfor- oxidation of Mn(II) at faster rates than abiotic processes mation into todorokite-like minerals. (Nealson et al., 1988; Takematsu et al., 1988; Tebo et al., 2004). Recent studies characterizing microbial Mn(II) oxi- 2. EXPERIMENTAL METHODS dation products reveal that they are exclusively X-ray amorphous, hexagonal, layer type Mn oxides with nano- 2.1. Biogenic Mn oxide production particle size similar to d-MnO2 (Bargar et al., 2005, 2009; Webb et al., 2005a,b; Miyata et al., 2006; Saratovsky Biogenic Mn oxides were produced by cultures of Pseudo- et al., 2006; Villalobos et al., 2006). Reaction of Mn(II) monas putida strain GB-1, provided by B.M. Tebo (Oregon and/or coexisting ions with the primary biogenic Mn oxide Health and Science University). Bacteria were grown in mineral yields abiotic secondary products, including 10-A˚ 500 mL L. discophora media in 1800 mL Erlenmeyer flasks Na phyllomanganate, feitknechtite, hausmannite and man- at 30 °C and 200 rpm in a temperature-controlled incubator ganite (Mandernack et al., 1995; Bargar et al., 2005). The with an orbital shaker. The Leptothrix media contained occurrence of diverse Mn oxides in surface environments 0.5 g LÀ1 yeast extract and casamino acids, 1 g LÀ1 glucose, may result from secondary products of biogenic Mn oxida- 10 mM HEPES buffer (pH 7.5), 2 mM CaCl2, 3.3 mM tion (Tebo et al., 2004; Villalobos et al., 2003, 2006; Bargar MgSO4, 3.7 lM FeCl3 and 1 mL trace element solution et al., 2005, 2009). (10 mg/L CuSO4Á5H2O, 44 mg/L ZnSO4Á7H2O, 20 mg/L The conversion pathways of biogenic Mn oxides into CoCl2Á6H2O, and 13 mg/L Na2MoO4Á2H2O) (Boogerd and other Mn oxides, especially tunnel structure Mn oxides de Vrind, 1987). Inoculum cultures were prepared by growing (e.g., todorokite), remains poorly understood. Although bacteria from a L. discophora agar plate in MSTG media todorokite is often found associated with Mn oxides of (2 mM (NH4)2SO4, 0.25 mM MgSO4, 0.4 mM CaCl2, microbial origin in ocean nodules, the pathways and mech- 0.15 mM KH2PO4, 0.25 mM Na2HPO4, 10 mM HEPES, anisms of todorokite formation from biogenic Mn oxides in 0.01 mM FeCl3, 0.01 mM EDTA, 1 mM glucose, and 1 mL nature are currently unknown (Burns and Burns, 1978b; trace metal solution) for 12 h at 30 °C(Parikh and Chorover, Siegel and Turner, 1983; Mandernack et al., 1995; Post, 2005). Cells were harvested after 19 h, via centrifugation at 1999; Buatier et al., 2004; Bodei et al., 2007). This is largely 10,000 RCF, at which time the cells have a maximum oxidiz- due to difficulty simulating the geochemical processes in- ing capacity. The harvested cells were rinsed with a solution volved in the mineralogical transformation from layered, of 10 mM HEPES at pH 7 to remove metabolites from the biogenic Mn oxides into tunnel structure Mn oxides. These spent media. The cells harvested from each 500-mL culture difficulties stem from the length of time these processes take were re-suspended in 1 L of autoclaved 50 mM NaCl and at room temperature (Cui et al., 2006); additionally identi- 10 mM HEPES at pH 7. Filter-sterilized MnSO4 solution fication of poorly crystalline phases in a mixed system is was added to the above solution after autoclaving to a final problematic.